How did warning coloration evolve?

June 5, 2023 • 9:30 am

Aposematic coloration, often called “warning coloration”, is the presence of bright or conspicuous colors or patterns in animals that are toxic, noxious, dangerous, or poisonous to predators. Here’s an example from Wikipedia, the granular poison frog (Oophaga granulifera). Like many dendrobatid frogs, this has a number of poison alkaloids in its skin, and they have been used in Central and South America to tip arrows or darts, which can kill mammals. Any predator that tried to eat one of these would probably be dead, or at least very ill.

My own frog, Atelopus coynei, looks conspicuous too [but see Lou Jost’s comment below], and may be toxic, but I don’t think people know anything about that:

Atelopus coynei. Photo: Jordy Salazar/EcoMinga

But of course far more animals than amphibians are aposematic. The skunk advertises its toxicity with a pair of conspicuous stripes. Many insects, like ladybugs and some leipidopterans, are also aposematic and toxic, including at least one bird species: see here for a Google image search of aposematic animals.

The colors and patterns, as the name implies, gives their bearers an evolutionary advantage over their presumably camouflaged ancestors, for predators will deliberately avoid the pattern, usually because they’ve learned to recognize and stay away from it because of previous unpleasant experiences. (The avoidance can also be evolved rather than learned, as you’ll see if you think about it. Even if eating one of these kills you, individual predators having less of a propensity to attack the pattern would be favored.)  Usually, however, learning is involved.

But to get that advantage, the aposematic species has to be sufficiently numerous to afford predators a chance to learn and then avoid the next aposematic animal. And this creates an evolutionary problem.

We are pretty sure that aposematic species evolved from camouflaged ones. To get the warning coloration started, there have to be mutations in the camouflaged population that produce individuals with bright colors and patterns, at least in incipient form.

And that’s the rub: the first mutant individual stands a higher chance of being attacked and killed than do cryptic individuals. Even if it’s toxic, it may still get killed or injured by being attacked for being a novel, conspicuous creature.  So how does the adaptation ever spread through the population from a rare initial state?

Previously, as described in the excellent Nature News & Views summary by Tim Caro below (click to read), we had a few answers:

1.) The trait could evolved by kin selection in gregarious animals. While the first mutant individual might be attacked, it might be part of a group of relatives that share that aposematic mutation. Assuming the predator learns to avoid the pattern after killing or hurting the first individual, it would avoid its similarly-colored kin, and that is a form of kin selection on the color/pattern genes that could make them spread.

2.) The trait could have evolved from a state that was conspicuous but not as conspicuous as the animals above. But this runs into the same problem as #1!

3.) The attacked aposematic mutant could avoid being killed by the predator because it smells or tastes bad, or is injured only slightly. If the predator learns from one experience (and some do), then that individual would henceforth be protected from predation, perhaps giving the mutant color/pattern gene an advantage. This seems somewhat likely, and could be tested by exposing naive predators to aposematic prey.

4.) Predators might avoid novel colors or patterns in general since the hunters have a search image for edible species. As Caro says, there’s some evidence for this, too.

But now, in his summary of the original paper, Caro describes a fifth hypothesis that is described in the Science paper below that.  The authors test this interesting hypothesis using phylogenetic data, and it seems to be supported.

Click the original Science paper below to read about the novel hypothesis for the evolution of aposematism. The authors test it in amphibians, but may hold for other creatures as well. You can also find the pdf here , and the reference is at the bottom. 

Again, I’ll try to be brief, but may not succeed. The authors’ hypothesis, which is very clever, is that full aposematic coloration may have evolved, at least in amphibians from an earlier state where it wasn’t clearly visible to predators. This could involve the colors/patterns starting their evolution on the BOTTOM (ventral) side of the animal, which wouldn’t draw attention until the animal was attacked, at which point it could flash its pattern and possibly startle the predator (the predator could also learn from a brief encounter that the prey was toxic).  And the bottom-colored state could itself be of two types: small patches on the ventral surface (PV) or a fully colored ventral surface (FV). This is in contrast to an animal that is fully colored all over its body.

Once the predator started learning what the color/pattern means from the animals that had it on their belly, then the color could evolve to cover the animal, making it fully aposematic.

But how do you test this hypothesis? Well, you could see if predators learn to avoid toxic amphibians that had color patches painted on their belly, but there are few amphibians that are toxic and lack aposematic coloration. No, the authors tested their hypothesis by doing phylogenetic reconstruction: they used living species and their known family tree to deduce what the color/pattern of the ancestors were. This kind of reconstruction, which makes sense if you have enough data, is increasingly used to study evolution.

And so Loeffler-Henry et al. did a big reconstruction of the evolutionary history of amphibians, many of whom were aposematically colored. They used 1106 species, putting each in one of five evolutionary categories:

species cryptic (camouflaged; “cry” in photo below)
species PV (ventral side partly aposematic)
species FV (ventral side fully aposematic)
species fully aposematic all over its body (“conspicuous” or “con” in photo below)
species polymorphic (some individuals are aposematic, others not). There aren’t many of these, and I won’t go into why they are supposed to exist.

Here’s a photo from the paper showing four of the five states (a polymorphic species isn’t shown):

Part of paper’s caption: Cry: cryptic; PV (partially conspicuous venter): cryptic dorsum with conspicuous color present as small patches on normally hidden body parts; FV (fully conspicuous venter): cryptic dorsum with conspicuous colors fully covered on the venter; Con: conspicuous

And here’s the reconstruction of the phylogeny showing the position in the family tree of each of the five states. Click to enlarge:

(From paper): Fig. 2. Ancestral state estimation of each color state (N = 1106 species) in frogs and salamanders. Pie charts at each node show the probabilities of ancestral states. The ancestral state of frogs and salamanders is likely to be cryptic coloration. The hidden color signals (PV and FV) are widespread and have evolved multiple times in different lineages. PV: cryptic dorsum with conspicuous color present as small patches on normally hidden body parts; FV: cryptic dorsum with conspicuous colors fully covered on the venter. See table S11 for photo credits.

There’s a pie diagram at each node of the tree showing the probability that that ancestor had one of the five states scored. I won’t go into the methods for deriving probabilities (in truth, I don’t understand them); but her are the salient points:

1.) Ancestors tend to be cryptic (camouflaged; gray dots), with the possible exception of some salamanders. This comports with the evolutionary view that aposematic coloration was not an ancestral condition but evolved as a defensive adaptation to deter predators.

2.) Full aposematism—the orange state—didn’t appear until later in amphibians, and

3.) . . . it did so generally going through an intermediate state of aposematic coloration on the belly (purple and red species)

4.) The preponderance of purple circles earlier than red ones suggests that the condition of full ventral coloration was preceded in time by the evolution of partial ventral coloration: patches of color that could be flashed but are still less conspicuous to predators than fully belly coloration. This suggestion is supported by statistical analysis of the likelihood of the models, but I’ll skip that.

Now this is an analysis of amphibians, but could apply equally well to other species. In fact, many butterflies that have warning coloration have it on their rear wings, which are covered up when they’re resting. It’s only when they fly, or when a predator startles them, that the aposematic coloration is revealed. Here’s an example: an aposematic butterfly from Ray Cannon’s Nature Notes. It’s the common birdwing (Troides helena), known to be very poisonous since the larvae feed on plants containing toxic aristolochic acids.

And here’s a fully aposematic butterfly:

(from site): Altinote dicaeus callianira – its distinct pattern advertises its unpalatability. Photo: Adrian Hoskins

For a long time the evolution of aposematic coloration posed the problem of what evolutionists call an “adaptive valley”: how do you get from one adaptive state (toxic but camouflaged) to a presumably more adapted state (toxic and brightly colored), when the intermediate evolutionary stage (the first mutant individual) was at a disadvantage: mired in an adaptive valley?  This could not occur by natural selecction since selection cannot favor the less adapted (here, “less avoided”) individuals.

The authors propose a solution to this: an adaptive valley wasn’t crossed because the intermediate state—ventral coloration—did confer a selective advantage on the first mutant individuals.

The authors end the paper by suggesting that their scenario could apply to many species; and it well could:

. . . macroevolutionary studies on animal coloration should take into account these underappreciated hidden signals, which are both common and widespread across the animal kingdom, to advance our understanding of the evolution of antipredator defenses. Indeed, many animal taxa such as snakes, fishes, and a variety of arthropods (see fig. S12 for example groups) include species that are cryptic, are aposematic, and have hidden conspicuous signals. We therefore encourage follow-up studies in other taxa to evaluate the generality of the stepping-stone hypothesis as a route to aposematism.


Loeffler, K., C. Kang, and T. N. Sherratt.  2023. Evolutionary transitions from camouflage to aposematism: Hidden signals play a pivotal role. Science 379:1136-1140. DOI: 10.1126/science.ade5156

Readers’ wildlife photos and story: the gruesome manipulation of hosts by parasites

April 20, 2023 • 9:45 am

Fortuitously, when I hadn’t prepared any posts for today that require my neurons to work, reader Athayde Tonhasca Júnior came through with one of his patented text+photo stories, this time a fascinating one about how opportunistic natural selection can create predator/parasite niches within niches in completely unexpected and astonishing ways. This hierarchy was wonderfully expressed in the short poem “Siphonaptera” (the order in which fleas are placed) by British mathematician Augustus De Morgan:

Great fleas have little fleas upon their backs to bite ’em,
And little fleas have lesser fleas, and so ad infinitum.
And the great fleas themselves, in turn, have greater fleas to go on;
While these again have greater still, and greater still, and so on.

Athayde’s text is indented, and click on the photo to enlarge them.

The body snatchers

by Athayde Tonhasca Júnior

Family feuds abound in history and in the tabloids, but things got really out of hand with the offspring of Egyptian gods Geb (Earth) and Nut (sky). As the first-born, Osiris was naturally chosen to be the ruler of the world. But his brother Set didn’t care one bit for this undemocratic arrangement, so he decided to despatch Osiris to the Underworld. So he set out a murderous plan worthy of an Agatha Christie story. Set first commissioned a beautiful casket, tailored to fit a body with Osiris’ exact measurements. Set then organised a magnificent banquet, inviting heavenly celebrities and bro Osiris. When they were all done with the eating and drinking, Set announced a surprise. The casket was brought in, and the host told his guests that whoever could fit inside, could take it home (an odd gift to us, perhaps, but who are we to judge Egyptian gods?). One by one the guests climbed into the casket, which was too small or too big – until Osiris had a go at it. He laid down inside the casket, which, to his glee, fit him perfectly. Set’s trap was set; he slammed the casket’s lid shut and locked it, killing his sibling. Later Set retrieved Osiris’ body and chopped it into small pieces.

The Mummy (1932) escaped from his sarcophagus, but no such luck for Osiris. Art by Karoly Grosz, Wikimedia Commons:

Set’s shenanigans were the perfect inspiration for naming a new species from the genus Euderus, a small group of parasitic wasps in the family Eulophidae. Most Euderus species are moth and beetle parasitoids, but the wasp discovered by Egan et al. (2017) in Florida (USA) is peculiar, to say the least. Its host, Bassettia pallida, is itself a parasitic wasp, but of a different kind: this species is one of the many gall wasps or cynipids (family Cynipidae), which lay their eggs in oaks (Quercus spp.) and less commonly in related plants (family Fagaceae). The egg-laying induces the plant to produce a gall, which is an abnormal growth resulting from increased size or number of cells (galls can also be caused by tissue feeding or infections by bacteria, viruses, fungi and nematodes). Cynipids trigger their host plants to produce nutritious tissue inside their galls, which become ideal places for a larva to grow: there’s nothing better for one’s survival than a cosy, safe and nourishing nursery.

Oak galls or oak apples, growths resulting from chemicals injected by the larva of gall wasps © Maksim, Wikimedia Commons:

In the case of B. pallida, it induces the formation of galls inside stems of sand live oak (Q. geminata) and southern live oak (Q. virginiana). Each of these galls is called a ‘crypt’. So appropriately, B. pallida is known as the crypt gall wasp. When the adult wasp completes its development, it chews an exit hole from inside its woody quarters and flies away.

(a): a crypt gall wasp; (e): adults’ exit holes © Weinersmith et al., 2020:

Life looked good for the crypt gall wasp in the southeastern United States—until we learned about the machinations of its recently discovered enemy. The Eulophidae parasitoid locates a crypt and pierces it with its ovipositor, laying an egg inside the chamber, near or into the developing crypt gall wasp. We don’t know exactly what goes on inside the chamber, but the outcome is not good at all for the crypt gall wasp. When it tries to chew its way out, it’s no longer able to create a hole big enough to fit its body: the wasp becomes entrapped inside its crypt, Osiris-like. During its failed attempt to get out, its head blocks the exit hole. All the better for the parasitoid larva that hatched inside the crypt: it can feed at leisure on the host’s weakened body. On completing its development, the adult parasitoid wasp chews through the host’s head plug and comes out to the big wide world. So there was no better name for this species than Euderus set, the crypt-keeper wasp.

JAC: Isn’t that an amazing story? I’m sure we don’t know how the parasitoid disables the gall wasp in this way. Imagine the genetic changes involved in this complex evolution, involving the parasitoid’s egg-laying and multiple behaviors of its larval stage. But that’s a passing expression of amazement; let’s continue with Athayde’s tale:

(c): a crypt-keeper wasp pupa in a chamber made by a crypt gall wasp; (f): an exit hole plugged by the head capsule of a dead or dying crypt gall wasp; (g): a crypt gall wasp head capsule chewed through by an exiting crypt-keeper wasp © Weinersmith et al., 2020.

The relationships between oaks and these wasps are examples of host manipulation, which happens when a parasite influences the host’s behaviour or physiology to its (the parasite’s) advantage. The crypt gall wasp induces its host plants to produce galls for its benefit, and in turn the crypt-keeper wasp forces its host into becoming trapped and an easy meal for the parasitoid’s larva: the manipulation of a manipulator is known as a hyper-manipulation, an uncommon phenomenon.

A female crypt-keeper wasp, a hyper-manipulator © Egan et al., Wikimedia Commons.

There are many cases of host manipulation, and the zombie-ant fungus described by the co-author of the theory of evolution by natural selection Alfred Russel Wallace (1823-1913) is one of the better known. This fungus (Ophiocordyceps unilateralis) induces its host ants to climb up the vegetation and clamp their mandibles around a twig or leaf vein. An infected ant will stay put, rain or shine, while the fungus grows inside it. After 4-10 days the ant dies, the fungus grows a ‘stalk’ (stroma) from the ant’s head and releases spores that will infect ants walking about on the forest floor.

A dead Camponotus leonardi ant attached to a leaf vein. The stroma of a zombie-ant fungus emerges from the back of the ant’s head © Pontoppidan et al., 2009:

The more researchers look into it, the more they find cases of host manipulators such as the Darwin wasps Hymenoepimecis spp., which parasitize several species of orb-weaving spiders in the Neotropical region. A female wasp stings and temporarily paralyses her victim, laying an egg on its abdomen. The emerging larva bites through the spider’s cuticle and feeds on its ‘blood’ (haemolymph). The spider carries on with its life, building webs and catching prey, but the growing parasitoid takes its toll; eventually it kills its host.

L: A H. heidyae egg attached to a Kapogea cyrtophoroides. R: Third instar H. heidyae larva feeding on a recently killed spider; the inset shows details of the dorsal hooks used by the larva to cling to its host © Barrantes et al., 2008.

But shortly before the spider’s demise, somehow —probably by hormone injection—the larva takes command of the host’s behaviour. The spider builds a cocoon web made of thickly woven silk, which doesn’t look at all like a normal web. The spider dies, the larva enters the cocoon and completes its development. Some days later, the adult wasp emerges and flies away.

a. A normal K. cyrtophoroides web; b. The web’s hub; c. A cocoon web induced by the parasitoid; d.  Central section of the cocoon web and the wasp’s cocoon © Barrantes et al., 2008.

Parasitic wasps are not deterred by the defences of hosts such as Anelosimus eximius. This is one of the few species of social spiders; they build massive tent-like nests that shelter hundreds or thousands of individuals, who hunt together in raiding packs and even cooperate in raising their young (click the next link to watch their comings and goings). But in the Amazon region, A. eximius can’t evade the Darwin wasp Zatypota sp. A parasitized spider leaves the colony and builds its own cocoon-like web. It then becomes immobilised, so that the wasp larva can unhurriedly consume it. When finished with its meal, the larva enters the cocoon to complete its development. The larger the spider colony, the more chances of being parasitized; up to 2% of individuals become hosts to the parasitoid (Fernandez-Fournier et al., 2018).

L: A group of A. eximius in a communal web © Bernard Dupont, Wikimedia Commons. R: A 5-m long, 3-m high colony of A. eximius; photo by A. Bernard © Krafft & Cookson, 2012:.

A fierce looking H. neotropica and its larva feeding on an Araneus omnicolor © Sobczak et al., 2012.

Host manipulation seems to be much more common than we thought, so we shouldn’t expect pollinators to be safe from it. And they are not. The conopid fly (family Conopidae) Physocephala tibialis forces bumblebee hosts to bury themselves in the soil just before dying. The nematode worm Sphaerularia bombi, found throughout the northern hemisphere and South America, infects queens of several bumble bee species, castrating its host. And at least for the buff-tailed bumble bee (Bombus terrestris), the nematode also alters the bee’s behaviour (Kadoya & Ishii, 2015). An infected queen feeds normally, but does not breed or build a nest. Instead, she keeps flying into the early summer months, and by doing so she unintentionally helps to spread the nematode. Certainly many other cases of pollinators’ manipulation by parasites wait to be discovered because their effects can be subtle and inconspicuous.

CSI Garden: a post-mortem examination of a buff-tailed bumble bee found dying on a roadside pavement in England revealed an infestation by the host-manipulating nematode S. bombi © The Encyclopedia of Life:

Host manipulation can be seen as a form of extended phenotype (Dawkins, 1982; phenotype refers to a species’ observable characteristics resulting from the expression of its genes). By changing the host’s behaviour for its own benefit, the parasitoid – ultimately, its genes – expresses its phenotype in the world at large. In Dawkins’ own words, ‘an animal’s behaviour tends to maximize the survival of the genes “for” that behaviour, whether or not those genes happen to be in the body of the particular animal performing it’. The phenomenon would have deep consequences for natural selection, but the extent of extended phenotypes has been debated since the publication of Dawkins’ book.

If you are smugly assuming that behavioural puppeteering is for lower animals such as insects, you’d better think again. Some studies suggest that rodents infected with the protozoan Toxoplasma gondii become more active but sluggish in reacting to alarm signals; worse, they may become attracted to the smell of cat’s urine. If so, an infected mouse has a good chance of prematurely ending its days in a moggie’s maw – which was T. gondii‘s ‘intention’ all along, since cats are its ultimate host. And the plot thickens: infected cats excrete T. gondii spores in their faeces, which can make their way into other mammals. A 26-year study with grey wolves (Canis lupus) from Yellowstone National Park, Wyoming, USA, revealed that infected individuals – probably the result of contact with pumas (Puma concolor) – are bolder, more likely to become pack leaders and have better chances of reproducing (Meyer et al., 2022). In humans, toxoplasmosis, the infection caused by T. gondii, is widespread but usually does not have any symptoms. Most people don’t even know they have it, but all sorts of behaviour and mental disorders such as heightened aggression and Parkinson’s disease have been linked to the infection. The effects of T. gondii on rodents and humans have been disputed because data often show weak, inconclusive or no effects (Johnson & Koshy, 2020). In any case, our invulnerability to the manipulative power of parasites should not be taken for granted. Rephrasing the quote misattributed to Margaret Mead, always remember that in biology, Homo sapiens is unique. Just like every other species.

Invasion of the Body Snatchers (1956). Art by Allied Artists Pictures Corporation. Wikimedia Commons.

JAC note: I don’t think that in any of these cases of host manipulation (or any others that I’ve heard of) do we know the chemical and developmental basis of the manipulation. What does a fungus do to an ant to make it climb a stalk of grass, grip it tightly with its mandibles, and then die? How does the Darwin wasp manipulate the spider’s behavior to cause it to weave a cocoon-like web instead of its normal web—something good for the wasp? These are incredibly sophisticated manipulations that have evolved in ways we don’t understand.

If this is the work of a creator, he must have been a sadist!

Did The Selfish Gene damage public understanding of biology?

October 9, 2022 • 9:30 am

This morning Matthew sent me a tweet by “The Dialectical Biologist” (TDB), which astounded me. I don’t know who TDB is, but he/she identifies as “Biologist. Anti-hereditarian. Lewontin fan.” The anti-hereditarian bit explains some of the criticality in the tweet below, and it’s worth noting that Lewontin himself gave The Selfish Gene a very critical review in Nature in 1977 (free with the legal Unpaywall app).

Here’s the tweet (the second part is the important claim), and two of the six subsequent tweets explaining why TDB sees The Selfish Gene as “the most damaging popular science book of all time.”

I was, of course, Dick Lewontin’s Ph.D. student, and I loved and admired the man. But I have to add that his Marxist politics, which included views of an almost infinite malleability of human behavior, did affect his science, and I think his review of Dawkins’s book is marred by that ideology. If you read Dick’s review, you’ll see that, like TDB above, Lewontin objects to the lack of discussion of genetic drift, and to Dawkins’s supposed claim (one that he didn’t actually make) that every aspect of every organism was installed by natural selection, accompanied by  untestable “adaptive stories” about how it arose. (Lewontin calls this “vulgar Darwinism”.)

In short, Lewontin’s review was an abridged version of his paper with Steve Gould, “The Spandrels of San Marco and the Panglossian paradigm: A  critique of the adaptationist program.” That paper was valuable in correcting the excesses of hyperselectionism, pointing out other reasons besides selection for the appearance of organismal traits and behaviors, and implicitly demanding data instead of fanciful stories for natural-selection explanations. (There are many traits, however, like extreme mimicry, where there is no plausible explanation beyond natural selection on bits of DNA.)

It is misguided to fault Dawkins’s book for not dealing in extenso with genetic drift or the San Marco alternatives. The Selfish Gene is essentially a book about how natural selection really works. It’s not important that it doesn’t define “gene” in the way that TDB wants; in fact, biologists haven’t yet settled on a definition of gene! It’s sufficient, when regarding the phenomenon of natural selection, to define a gene as “a bit of DNA that affects the properties of an organism”. If those properties enhance the reproduction of the carrier (the “vehicle”), then the gene gets overrepresented in the next generation compared to the alternative gene forms (“alleles”). These selected bits of DNA act as if they were selfish, “wanting” to dominate the gene pool. That is a very good metaphor, but one that has been widely misunderstood by people who should be thinking more clearly.

The value in the book lies in its clear explanation of how natural selection acts largely (but not entirely) at the level of the gene, not the organism, the group, the population, or the species; its distinction between “replicators” (bits of DNA subject to natural selection) and “vehicles” (the carriers of replicators whose reproductive output can be affected by those replicators); that “kin selection” is, in essence, nothing really different from natural selection acting on the genes of an individual; and that, contrary to a naive “selfish gene” view, altruism can result from natural selection. Finally, it explains clearly the thesis (earlier adumbrated by G. C. Williams) that “group selection—selection on populations—is not a major source of adaptation in nature. (See Steve Pinker’s wonderful essay on the inefficacy of group selection published ten years ago in Edge.)

The Selfish Gene is the clearest explanation I know of how natural selection works, as well as an exposition of ideas like kin selection that were fairly new at the time of the book’s publication.  It also introduces the idea of “memes”, which I think is a distraction that has led almost nowhere in the understanding of culture, but that is just a throwaway notion at the end of the book. (You can see my critique of the meme framework in a review of Susan Blackmore’s book The Meme Machine that I wrote for Nature; access is free.)

Think of the book as an explanation for the layperson about how natural selection really works, and you’ll recognize its value. As far as “damaging” the popular understanding of science, that is a grossly misguided accusation. By explicating how natural selection really works, explaining some of its variants (like kin selection), and dismissing widespread but largely erroneous ideas about selection on groups, The Selfish Gene did the public an enormous service. While popularity is not always an index of a science book’s quality, in this case it is: many laypeople have written about how they finally understood natural selection after reading it.

I could, in fact, argue that the San Marco paper by Gould and Lewontin was damaging, too, by overly restricting the domain of natural selection and failing to adduce cases where drift or pleiotropy were not sufficient explanations for traits (mimicry is one), so that natural selection was the most parsimonious explanation. (In the latter part of his career, it was hard to get Steve Gould to even admit that selection was important, much less ubiquitous). But “San Marco” was itself valuable in dampening hyper-Darwinism, and in the main was a good contribution to  evolutionary biology. The Selfish Gene was, however, a much better contribution

I asked Matthew, someone who of course knows the ins and outs of evolutionary genetics, if he agreed with TDB’s negative assessment of The Selfish Gene. His reply:

Given I am giving a lecture tomorrow in which I tell 600 students they should all read it, I think not…

When I asked permission to reproduce his quote above, he said “sure” and also me the slide he’s showing his 600 students:

. . .and added this:

FWIW I also show them three views in the levels/units of selection debate (a philosopher who says it has to be genes as they are the only things that are passed down, Dick who says we can’t really know and Hamilton who says it’s complicated and it depends what you look at).
The next section of the lecture deals with social behaviour (hence the final line)
I invite those readers who have read The Selfish Gene to weigh in below with their opinion.

Patrick Matthew: the real inventor of the idea of natural selection?

August 5, 2022 • 9:15 am

Of the several independent assertions that constitute Darwin’s “theory of evolution” in On The Origin of Species, Darwin regarded the idea of natural selection as his most important and original. After all, it alone explained how naturalistic processes could lead to the remarkable adaptations of animals and plants heretofore seen as some of the strongest evidence for God. And although the idea of evolution itself had been broached by others before Darwin, including his own grandfather Erasmus, natural selection seemed to be sui generis.

Well, not entirely.  It was anticipated by several people, including the Scottish polymath James Hutton in 1794. But the most remarkable precursor to the idea of natural selection was published by Scottish horticulturalist and agriculturalist Patrick Matthew (1790-1874) as an appendix to his book On Naval Timber and Arboriculture (1831). Although the book was about how to build ships using wood, and what kind of wood to use, Matthew added a 28-page Appendix. In that Appendix were 29 sentences that laid out what he called “selection by the law of nature”, which bore a striking similarity to the idea made famous by Darwin 28 years later.

You can read Matthew’s appendix at Darwin Online, and some of the statements about his views of natural selection can be seen and discussed in context here, here, and here.

Here are two excerpts from Matthew’s Appendix:

THERE is a law universal in nature, tending to render every reproductive being the best possibly suited to its condition that its kind, or that organized matter, is susceptible of, which appears intended to model the physical and mental or instinctive powers, to their highest perfection, and to continue them so. This law sustains the lion in his strength, the hare in her swiftness, and the fox in his wiles. As Nature, in all her modifications of life, has a power of increase far beyond what is needed to supply the place of what falls by Time’s decay, those individuals who possess not the requisite strength, swiftness, hardihood, or cunning, fall prematurely without reproducing—either a prey to their natural devourers, or sinking under disease, generally induced by want of nourishment, their place being occupied by the more perfect of their own kind, who are pressing on the means of subsistence.

. . . There is more beauty and unity of design in this continual balancing of life to circumstance, and greater conformity to those dispositions of nature which are manifest to us, than in total destruction and new creation. It is improbable that much of this diversification is owing to commixture of species nearly allied, all change by this appears very limited, and confined within the bounds of what is called Species; the progeny of the same parents, under great difference of circumstance, might, in several generations, even become distinct species, incapable of co-reproduction.

The self-regulating adaptive disposition of organized life may, in part, be traced to the extreme fecundity of Nature, who, as before stated, has, in all the varieties of her offspring, a prolific power much beyond (in many cases a thousandfold) what is necessary to fill up the vacancies caused by senile decay. As the field of existence is limited and pre-occupied, it is only the hardier, more robust, better suited to circumstance individuals, who are able to struggle forward to maturity, these inhabiting only the situations to which they have superior adaptation and greater power of occupancy than any other kind; the weaker, less circumstance-suited, being permaturely destroyed. This principle is in constant action, it regulates the colour, the figure, the capacities, and instincts; those individuals of each species, whose colour and covering are best suited to concealment or protection from enemies, or defence from vicissitude and inclemencies of climate, whose figure is best accommodated to health, strength, defence, and support; whose capacities and instincts can best regulate the physical energies to self-advantage according to circumstances—in such immense waste of primary and youthful life, those only come forward to maturity from the strict ordeal by which Nature tests their adaptation to her standard of perfection and fitness to continue their kind by reproduction.

Well yes, that has variation, differential survival, culling of most individuals in a species, speciation, and adaptation—all features of Darwin’s own theory. It’s a remarkable anticipation of Darwin’s ideas.

Does this mean that Matthew deserves credit for the idea of natural selection? Only as an anticipation of Darwin’s far more thorough explication (Darwin, by the way, never read Matthews’ Appendix). Matthew deserves no more credit for natural selection as a popular idea than does Erasmus Darwin for evolution. Matthew’s ideas weren’t adopted, were almost never cited, had no influence in biology, and Matthew never realized until after The Origin was published (and sold out the printing in a single day) that he once had within his grasp The Big Idea that explained the design-like features of nature.

Nevertheless, several people have tried to diminish Darwin’s idea by pointing out that Matthew had it first—and that Darwin plagiarized it. The latest attempt is by Mike Sutton in this book published two months ago (click on image to go to Amazon link):

I haven’t read it, but according to Geoff Cole, a cognitive scientist at the Centre for Brain Science at the University of Essex, who reviewed the book in the latest issue of Evolution (click below for free access), Sutton’s book is a real hit job on Darwin.

The title of Sutton’s book clearly asserts that Darwin took credit for Matthew’s theory, and it’s true that once Patrick Matthew had read The Origin, he argued for his own precedence, even though Darwin had never seen the “incriminating” sentences above.  Sutton also claims that Matthew’s idea had real priority because Naval Timber was cited by others before 1859, but as Cole notes in a very critical but polite review, those citations were almost all to the book itself, not to the ideas in the Appendix.

Cole also notes Sutton’s ridiculous accusations of Darwin’s “plagiarism”:

What is most uncomfortable about Sutton’s thesis is his treatment and personal attack on Darwin. He suggests that Darwin ”was a plagiarist who lied repeatedly” and undertook “deliberate, knowing fraud”. Indeed, “the biggest science fraud in history”; fraud that Darwin supposedly hoped “nobody would notice”. Sutton also expresses suspicion about the chronic illness Darwin was known to suffer; a subject that many historians have written about (e.g., Hayman, 2009). From every single account of Darwin and how he went about his life, these “lies” are the complete opposite of what we know about the man. I have lost count of the number of times I have seen a scholar write that a particular event “is testament to his honesty”. As Browne (1985) stated, “By the time Descent of Man was published in 1871 reviewers were falling over themselves to congratulate Darwin’s “unassailable integrity and candour, and his “wonderful thoroughness and truthfulness” (Browne, 1985, p.257 & 258).

Every serious historian who’s studied Darwin’s life knows that he was neither a plagiarist nor a liar, although he did, understandably, want to preserve credit for his own ideas. After Matthew wrote a claim of his priority in The Gardner’s Chronicle in 1859, Darwin not only published an acknowledgement of Matthew’s precedence in the same magazine, but also inserted this long acknowledgment of Matthew’s work into the 3rd edition of On the Origin of Species:

In 1831 Mr. Patrick Matthew published his work on ‘Naval Timber and Arboriculture,’ in which he gives precisely the same view on the origin of species as that (presently to be alluded to) propounded by Mr. Wallace and myself in the ‘Linnean Journal,’ and as that enlarged on in the present volume. Unfortunately the view was given by Mr. Matthew very briefly in scattered passages in an Appendix to a work on a different subject, so that it remained unnoticed until Mr. Matthew himself drew attention to it in the ‘Gardener’s Chronicle,’ on April 7th, 1860. The differences of Mr. Matthew’s view from mine are not of much importance: he seems to consider that the world was nearly depopulated at successive periods, and then re-stocked; and he gives, as an alternative, that new forms may be generated “without the presence of any mould or germ of former aggregates.” I am not sure that I understand some passages; but it seems that he attributes much influence to the direct action of the conditions of life. He clearly saw, however, the full force of the principle of natural selection. In answer to a letter of mine (published in Gard. Chron., April 13th), fully acknowledging that Mr. Matthew had anticipated me, he with generous candour wrote a letter (Gard. Chron. May 12th) containing the following passage:—”To me the conception of this law of Nature came intuitively as a self-evident fact, almost without an effort of concentrated thought. Mr. Darwin here seems to have more merit in the discovery than I have had; to me it did not appear a discovery. He seems to have worked it out by inductive reason, slowly and with due caution to have made his way synthetically from fact to fact onwards; while with me it was by a general glance at the scheme of Nature that I estimated this select production of species as an à priori recognisable fact—an axiom requiring only to be pointed out to be admitted by unprejudiced minds of sufficient grasp.”

Cole explains patiently why Darwin should get nearly all the credit for the idea of natural selection. A few excerpts from Cole’s excellent review:

Who then should be credited with discovering the process by which evolution occurs? Matthew, Hutton, Maupertuis, Wells? Or anyone else who also chipped in? The answer is simple. Charles Darwin.

. . . A necessary condition of insight is that the knowledge must be reflected upon and placed within the appropriate context. Unless a person fully recognises what they have said, done, or found, no formal insight has occurred. There is no priority.

. . . I suspect Matthew was annoyed with himself, as I was with myself, for not realising the importance of what he had written. That may have been why he dedicated so much of his later efforts on his priority claim. If he had realised he would surely have submitted an academic paper outlining his theory; a paper that was only about the theory. Given fear of religious establishment, this could have initially been anonymously penned. He may have even published a book on the origin of all life forms and how the development of every single species can be explained. He would have also repeatedly used his phrase “the process of natural selection”, a phrase Sutton places great emphasis on, as opposed to the one time he did so in Naval Timber. As it was, there was no paper or book. There was no in-depth development of ideas about evolution and how it relates to divergence, heredity, the geological record, geographic distribution, classification, morphology, and embryology. No lengthy discussion of how there are problems and “difficulties” with his own theory. There was not 30 years of methodical work in which he used his theory to explain aspects of cross-pollination and movement in plants, not to mention work on human psychology, sexual behaviour, and emotions. There were no lengthy and numerous discussions with colleagues about his theory and when he should go public.

In fact, Sutton acts like a creationist, arguing that generations of evolutionary biologists have realized that Matthew should really get credit for the idea; but we have, because of our mindless adulation of Darwin, kept that quiet:

Essentially, Sutton has to explain why generations of evolutionary biologists and the like have never come to the same conclusion as himself. The usual explanation is that we are all involved in a “cover up” (p. 5) or part of the “Darwin Industry”, as Sutton calls it, in which a “loosely affiliated in-group of scientists, historians of science, other writers, publishers, editors, and journals, share a common goal to protect the perception of Charles Darwin as a genius science hero” (p. 10). But how This article is protected by copyright. All rights reserved. about this for an alternative explanation? Those generations of biologists have independently decided that there is nothing to see here, that Darwin should be honoured with discovering evolution. Furthermore, if a few sentences in which natural selection is referenced warrants priority, as Sutton seems to believe, then why pick out Patrick Matthew? Why not his predecessors, Hutton, Wells, or Maupertuis? In fact, shouldn’t Matthew be accused of plagiarism, having failed to acknowledge the fact that his ”own original child” was described at least 30 years before by various others?

Sutton’s book is his latest, in his decade-long, attempt to undermine Darwin’s priority. As all others before, this one will fail.

Of that there’s no doubt. Matthew’s independent musings about natural selection are a remarkable coincidence, but he didn’t make much of them, didn’t examine them further, and certainly didn’t try to integrate them into a grand theory of organic evolution. But judge for yourself: I hope you’ve read The Origin, so just peruse Matthew’s brief discussion and then ask yourself whether Matthew should get the lion’s share of the credit for the idea of natural selection.


One brief correction of Cole’s fine review: on its first page it describes Darwin as being “the ship’s naturalist” on the voyage of the Beagle. That’s a common misconception, for an “official” naturalist—the ship’s surgeon Robert McCormick—had already been designated. Darwin sailed on the Beagle using his own money, and his position was as both a “self funded naturalist” and also the “captain’s companion”. He was taken aboard largely to provide gentlemanly company for Captain FitzRoy, with whom he dined and conversed. Darwin’s researches and collections during the voyage were done on his own volition and enthusiasm.

Why does the skin on your fingers and toes wrinkle after immersion in water? A panselectionist answer.

June 22, 2022 • 9:45 am

All of us have noticed that after a period of immersion in water, the skin on both our fingers and toes wrinkles up, but not the skin anywhere else on our body. Here are two photos of the crenulated digits:

From The Conversation


This raises two questions:

a.) What is the mechanism for the wrinkling?

b.) Is there any usefulness or “adaptive significance” of the wrinkling? That is, did natural selection favor it because the wrinkles are useful. 

The two articles below, the first a new popular summary from the BBC and the second a year-old scientific paper discussing the “adaptive significance” of the wrinkling, suggest answers to both questions.

It turns out that we know the mechanism of wrinkling pretty well, but, despite the assurance of both articles, we still have no idea whether it’s an “adaptive” response to water or merely some epiphenomenon that makes no difference to our well being or reproductive output.  That both articles immediately look for an adaptive “reason” why natural selection promoted finger and toe wrinkling is an example of what Steve Gould called “naive pan-selectionism”: assuming that every feature has natural selection behind the evolution of that feature, and favoring the production of that feature—in this case, wrinkling.

Panselectionists often accept pretty scanty evidence as being supportive of their theory, and I think you can see that here.

Click on both screenshots to read the article; the pdf of the scientific article (in PLOS One; reference at bottom) can be downloaded here.



I’ll use facts from both articles, but quotes will be attributed to one or the other.

First, how long does it take to wrinkle up? It depends on the temperature, with 3.5 minutes in warm water to begin wrinkling (40º C or 104° F) and 10 minutes in tepid water (20º C or 68° F). But even in cool water we will wrinkle.

How does it happen? Scientists first thought that it was simple osmosis: the skin cells absorbed ambient water and that made the cells swell up, causing wrinkles. But then they noticed that if the median nerve in the arm is severed, there is no wrinkling. That rules out the osmosis theory as a complete explanation. Osmosis may contribute a bit to the wrinkling, but nerves and blood vessels are also involved. Author Davis of the PLOS ONE paper says this:

Explanations for the wrinkling of the skin include a passive response of the skin to immersion, or an active process that creates the wrinkles for a functional purpose. There is overwhelming evidence that finger-wrinkling is an active process. The small blood vessels of the fingertip constrict, which creates valleys in the skin surface, triggered by water entering sweat pores . Note that a passive explanation would usually assume that water absorbs into the skin, pushing up ridges. This vasoconstriction appears to occur most readily at a temperature of around 40° Celsius, or the temperature of a warm bath [2]. People with autonomic neurological conditions including Parkinson’s, cystic fibrosis, congestive heart failure or diabetic neuropathy may show abnormal or asymmetric wrinkling in the affected parts of the body.

Note that in the first sentence he conflates an “active process” with “an adaptation that has a functional purpose.” This isn’t necessarily true. We get wrinkles, gray hair, and liver spots with age, which are “active processes,” but that doesn’t mean those features are the direct products of natural selection. (What is the adaptive function of liver spots?). The BBC adds a bit more about the mechanism:

Wilder-Smith and his colleagues proposed that when our hands are immersed in water, the sweat ducts in our fingers open up to allow water in, which leads to an imbalance in the salts in our skin. This change in the salt balance triggers the firing of nerve fibres in the fingers, leading to the blood vessels around the sweat ducts to constrict. This in turn causes a loss of volume in the fleshy area of the fingertip, which pulls the overlying skin downwards so that it distorts into wrinkles. The pattern of the wrinkles depends on the way the outermost layer of skin – the epidermis – is anchored to the layers beneath it.

The involvement of nerves explains why some conditions that affect nerves (see first indented para above) affect skin wrinkling.

Let’s assume, then, that we have a pretty good idea of how this happens in fingers, though nobody says much about toes or the rest of the body. (Toes are also sorely neglected in the “adaptive” explanation.

Both sets of authors then set about explaining why natural selection would favor such wrinkling (again, they discuss only fingers, not toes). The experiment describe in the second link above, which gives results in line with previous studies, suggests that the wrinkled skin allows you to grab wet objects with more force than if your skin is unwrinkled and wet. And if your fingers are wrinkled, you’re likely to be in an environment where there are wet objects.  The purported mechanism for this is the same one for treads and valleys in tires: the “channels” in our finger wrinkles suposedly help squeeze out the water when we’re gripping a wet object, allowing better contact with the object. (But what about the toes?)

Davis, then, did a study estimating the strength it took to grip a small and initially DRY plastic disk under three conditions:

a. dry unwrinkled fingers

b. wet wrinkled fingers (note: they apparently didn’t use dry wrinkled fingers, but it’s not clear from the paper. In fact, if they used dry unwrinkled fingers, it would make the adaptive explanation less credible.)

c. wet unwrinkled fingers

Not did they use wet objects, which is crucial for their adaptive hypothesis, though of course gripping a plastic disk with wet wrinkled fingers will make the object wet. Note also that the object is small and light (the BBC says it weighed as much as a couple of coins).

I won’t go into the detail to measure force, but they had an apparatus that measured both grip strength and the ability of the subject to lift up the object and hold it sufficiently tightly so it could be manipulated to follow a computer track. Here’s a photo from the paper:

(From paper): Fig 1. Picture of the equipment in use. The participant is gripping a load cell between finger and thumb. The participant’s task is to pull up on the second load cell to match a force trace that appears on the laptop monitor. The current load force is shown as a red circle, and the history of the participant’s force is shown as a trail of green dots.

The results: people with wet wrinkled fingers and those with dry fingers had similar grip forces, but those with wet, unwrinkled fingers needed significantly more force to grip the disk. Here’s one graph (just look at the top three lines) showing no significant difference between wrinkled-finger force (red) and dry-fingered force (purple), but significantly more force needed using wet, unwrinkled fingers. (The paper give statistics). This shows no real benefit of wet, wrinkled fingers over dry fingers when gripping the disk, but if your fingers are wet and unwrinkled, it’s harder to grip (the plastic get slippery).

(From paper): Fig 2. Comparison of performance across conditions. Mean grip force (thinner traces) and load force (thicker traces) when participants tracked a load weight target (black line). Participants with wrinkled fingers produced a grip force that did not differ from that used by people with dry fingers in the static hold phase, however people with wet but non-wrinkly fingers used a significantly higher amount of grip. The shaded area indicates the pointwise ±1 standard error of each mean trace. Lines below the trace indicate the attack phase (A) of the trial, the static phase (S) and the decay phase (D).

Here’s another graph that shows pretty much the same thing, but showing the grip force needed to sustain the load of the plastic disk under the same three conditions but with varying “load force” (weight, which could be manipulated). Green is wet, unwrinkled fingers, red is wet, wrinkled fingers, and blue is dry unwrinkled (normal) fingers:

(From paper): Fig 4. Relationship between grip and load force in Dry, Wet and Wrinkly conditions. This illustrates the grand mean of the grip and load forces for the whole duration of the trail, minus the first 1000 ms. The target force is shown as a dashed line. The three grip force traces lie above this line, indicating the safety margin. The ‘easiest’ condition, Dry (blue trace) follows the target force most closely. The ‘hardest’, Wet (green trace), shows a higher safety margin, and looser coordination. Participants with Wrinkly fingers (red trace) lie between the two.

Wet unwrinkled fingers require more force to hold the disk than do dry ones. Wet, wrinkled fingers aren’t superior to either, but intermediate between them. (No statistics are given, but another graph implies that none of the differences between the lines in the plot right above are significant.)

The overall conclusion is not strong. Clearly, wet unwrinkled fingers make it harder to grip a smooth plastic object than either dry fingers or wet wrinkled fingers (DUH), but wet wrinkled fingers don’t make it easier to grasp an object than dry unwrinkled fingers. In other words, any advantage of wrinkling is only when it’s compared to wet unwrinkled fingers. Otherwise, dry fingers grasping a dry object are marginally (and nonsignificantly) better than wet, wrinkled fingers.

What can you conclude from this? I’d say, “not much”, but the author of both the BBC article and of the paper seem to think that wrinkling is an adaptation that evolved in our ancestors to enable them to grip objects under wet conditions:


This suggests that humans may have evolved fingertip and toe wrinkling at some point in our past to help us grip wet objects and surfaces.

“Since it seems to give better grip under water, I would assume that it has to do with either locomotion in very wet conditions or potentially with manipulating objects under water,” says Tom Smulders, an evolutionary neuroscientist at Newcastle University who led the 2013 study. It could have given our ancestors a key advantage when it came to walking over wet rocks or gripping branches, for example. Alternatively, it could have helped us when catching or foraging for food such as shellfish.

From the paper:

Grip and load force coordination is an important aspect of object handling. The ability to generate the correct amount of grip force for a given load means that the minimum necessary amount of energy is used by the muscles that control the fingers and hands, and means that objects are less likely to be dropped or to be crushed. Efficient grip force coordination is seen in many extant primates, and is likely to have evolved early in the primate lineage [13]. The grip force required to stabilise a wet object is greater than the force required for a dry object, since the coefficient of friction of the digit-object interface is reduced [8]. It would therefore benefit an animal to gain an advantage in handling wet objects, as this would increase success in hunting and foraging in watery environments. The skin of the fingertip is already adapted for regulation of moisture at the contact surface [14]. Fingertip wrinkles would seem to afford an enhanced advantage in object handling, and may plausibly aid travel and clambering in wet areas, especially if combined with wrinkled toes.

Ergo, it helped us “hunt and forage in watery environments.” But this raises a number of questions:

a.) If you’re hunting or foraging in a watery environment, but your hands have been immersed for fewer than 20 minutes so they’re unwrinkled, you’re better off gripping a dry object with dry hands instead of wet ones. You have an advantage with wrinkled fingers only if they’ve been underwater long enough to get wrinkled, and that advantage is only over unwrinkled wet fingers so long as you’re gripping an object that is itself wet, like a plastic disk that your fingers have wetted.  If you’re trying to grab a dry object when your hands are wet and wrinkled, you’re worse off than when using dry hands.

b.) They did not test the three conditions when gripping large dry objects like a tree branch or an animal, which may not behave like plastic disks! This is essential if you think that either grabbing dry objects was important for our ancestors even when our fingers were wrinkled from having been immersed in water.

b.) We did not evolve in a watery environment; the “aquatic ape” hypothesis has long been dispelled. As for our relatives, the BBC article says “only one other primate has so far been found to have water-induced wrinkling of the fingers—Japanese macaques.” (Naturally, they show a photo of a macaque sitting in water.) I’m not sure if other primates have eve been tested (no such tests are referenced), but if chimps, bonobos, and orangs show finger wrinkling, that would imply that it did NOT evolve to enhance grip strength in watery environments. These primates don’t live in those environments!

d) What about doing the study with dry wrinkled fingers? (You quickly dry them before grasping the object.) The adaptive hypothesis would predict that there would be no grasping advantage of dry wrinkled fingers over dry unwrinkled fingers. They didn’t do that experiment (as far as I can see).

e.) What about the TOES? They get wrinkled too. The paper posit that wrinkled toes would aid “travel and clambering in wet areas”, but that is pure speculation—not even a hypothesis. It could be fairly easily tested, but wasn’t.

f.) If wrinkly skin is pretty much as good as dry skin for gripping almost anything, why don’t we have permanently wrinkled skin? Author Davis has an answer:

A previous study of object manipulation with wrinkled fingers found that wet objects were moved more quickly when the fingers were wrinkly compared to dry [15]. Importantly, there is no difference in tactile sensitivity in wrinkled fingers compared to dry [16], meaning that people are not trading off acuity for friction at the fingertip. It is therefore reasonable to wonder why healthy people do not have permanently wrinkled fingers. The answer presumably lies in the changes in the mechanical properties of the finger tissues, where there may be lower shear resistance when the finger is wrinkled [17]. Previous studies have also suggested differences in manipulation across the lifespan [1820]; the present results show age-related effects, although they are rather weak in this sample. Our journey through life leads us to develop strategies for handling familiar and unfamiliar objects, so it seems likely that strategic changes, along with sensory and motor changes, will affect how children and adults perform tasks with handheld objects [21].

Here we have ultimate pan-selectionism: if your hypothesis fails to explain another phenomenon, you simply make up a reason why that’s also adaptive. In this case, Davis posits “lower shear resistance” for wrinkled fingers, which for a reason he fails to specify must confer a disadvantage (presumably because you can’t hold onto an object as tightly).

I’m not at all convinced by this explanation or the supporting data, as they’re contradicted by evolutionary observations and by the absence of data on wrinkled toes. As the BBC says, some believe that wrinkling “could just be a coincidental physiological response with no adaptive function.” (Go have a look at that link!). I am one of those skeptics. What surprises me is that that statement is the sing caveat (and doesn’t reprise what’s at the link) in a whole article pushing the “adaptive wrinkling in wet environments” hypothesis.

Other venues have also picked up this result, and I guess they are either overly credulous or didn’t read the paper carefully enough. Or they didn’t ask probing questions.

h/t: Peter


Davis NJ (2021) Water-immersion finger-wrinkling improves grip efficiency in handling wet objects. PLOS ONE 16(7): e0253185.

How Asian honeybees kill their fearsome hornet predators

May 10, 2022 • 12:45 pm

I can’t remember why I opened the natural-selection chapter in Why Evolution is True (chapter 5: “The Engine of Evolution”) with the story of the Asian giant hornet (Vespa mandarina) and of the counterdefense of its prey of native honeybees. (The European honeybee, more recently introduced into Asia, has not evolved such a bizarre and amazing defense.)  The giant hornet is much to be feared by both honeybees and humans: it’s as big as your thumb, and several humans (and millions of bees) die from its attacks every year.

Since you all should have a copy of WEIT (as Hitch would say, “Available at fine bookstores everywhere”), I won’t recount the story of the native honeybees’ defense, but it involve luring the voracious hornet scout into the bee nest and the cooking it to death:  surrounding it with a ball of vibrating bee bodies that raises the ball’s internal temperature to 117 degrees F (47°C): a temperature that kills the wasp but not the bees.

I suppose I put that story in because it’s a stunning example of the power of natural selection to shape behavior (in both wasp and bee), and not many people knew about it. Now I hear that a lot of readers especially liked that story. It is a true one, and in this segment from BBC Earth, you can see the nefarious hornet scout discovering a hive of native honeybees.

The scout marks the hive with pheromones and usually flies back to recruit a swarm of fellow hornets to return to the nest to destroy it: a process that can take only a short while as the wasps  nest in minutes, decapitate adult bees and steal their honey and and bee grubs. But, as I relate in the book, sometimes, as here, the hornet scout never gets back to its own nest because of the counterdefense. The native bees lure it inside and cover it with vibrating bees that kill it.

This video is, of course, far more vivid that what I could say in words, so I want to show it here. But imagine the sequence of evolutionary steps that produced this defense!

If you want to see how these hornets slaughter the non-native European honeybees, watch this gruesome attack (each wasp can kill 40 bees per minute!). I’m sure I’ve shown this video somewhere in the distant past.

Now if you’ll excuse me, i’ll go home to rest.

Ivory poaching imposing selection on elephants to evolve shorter tusks

October 24, 2021 • 9:30 am

Here we have a case of selection by humans—killing elephants that have tusks because ivory is so valuable—increasing the frequency of tuskless African elephants in Mozambique over a 28-year period. (As we’ll see, only the proportion of tuskless females increased.)  We have similar examples from other species, as in the reduction of horn size in bighorn sheep hunted for their horns as trophies, and the reduction in the size of some fish due to commercial fisherman going after the big ones.

Is this artificial or natural selection? Well, you could say it’s artificial selection because humans are doing the choosing, but after all human are part of nature. And this selection was not conducted to arrive at a given end. Dachshunds were selected to look like hot dogs to root out badgers in their burrows, but the reduction of tusk size in elephant, or horns in sheep, was not a deliberate target of selection, but a byproduct of greed. So I would hesitate to characterize this as artificial selection, since it’s not like breeders choosing a given characteristic to effect a desired change. In fact, the evolutionary change that occurred is the opposite of what the “selectors” wanted.

You can find the article in Science by clicking on the screenshot below, or get the pdf here.  There’s a two page shorter take that’s an easier read, “Of war, tusks, and genes,” here.

The phenomenon: a civil war in Mozambique from 1977 to 1992, which increased the frequency of tuskless female elephants from 18.5% to 50.9%, nearly a threefold increase. Why? A model showed that such a change (which occurs among generations, so it’s not just selective killing within a generation) must have been due to natural selection rather than genetic drift. The killing was motivated by a desire to get money to fund the conflict.  A female without tusks had five times the chance of surviving as a tusked female. That imposed strong selection in favor of tuskless females.

Usually, tuskless elephants are at a disadvantage, for tusks are multi-use features, employed for defense, digging holes for water, male-male competition, and stripping bark from trees to get food. But the natural selection to keep tusks in females was weaker than the “artificial selection” by humans against tusks.

Here’s a photo of a tuskless vs. a tusked female:

Photo by Finbarr O’Reilly for The New York Times

And the only kind of male that we see: ones with big tusks (tusk size varies, of course, as they continue to grow as the elephant lives). Tusks are homologous with our incisor teeth.

The authors first tried to determine the genetic basis of having versus lacking tusks. It turns out that, by and large, tusklessness behaves not as a complex trait caused by changes in many genes of small effect, but as a single dominant mutation on the X chromosome (like us, elephant males are XY and females are XX). Further, the dominant mutation causing tusklessness is lethal in males, killing them before birth. (This is probably not because the tuskless gene form is itself lethal, but is closely linked to a gene that is a recessive lethal.)

So here are the “genotypes” of the elephants. I’ve used “x” as the gene form on the X chromosome that produces tusks, and “X” as the alternative dominant allele that makes you tuskless.

Males: All have tusks and are thus xY. (Males have only one X chromosome and also a Y.) The XY genotype is lethal, so we never see males carrying the tuskless gene form (XY). Ergo, there are no tuskless males.

Females: We see two types:

Tuskless: Xx. These females will lose half their male offspring because when mated to an xy male (the only viable type), they produce half xY males, which are tuskers, and half XY males, which are lethal. Thus a population of tuskless females will produce a sex ratio in their offspring skewed towards females, which is what is observed.

We never see XX tuskless females because they’d have to inherit one “X” from from their fathers, but that XY genotype is lethal.

With tusks: xx.

There are a few complications, as other genes are involved (for example tusked mothers, who are xx, produce only 91% of tusked daughters when you’d expect the xx by xY cross to produce 100% xx (tusked) daughters. So things are not quite so simple, but in general a single gene seems largely responsible for the tuskless condition. (You might expect this, because if many genes were involved you simply wouldn’t get females lacking tusks: you’d get females with slightly smaller tusks, who would still be killed for their ivory. It would thus take many generations instead of a couple to raise the frequency of tuskless females.)

I won’t go into the gory genetic details, but the authors sequenced entire genomes from tusked and tuskless males and females and looked for signs of natural selection on some genes, comparing the tusked versus tuskless females. (One sign of rapid selection for tusklessness, for the cognoscenti, is the presence of DNA bases recurrent and common near the gene causing tusklessness.)

The researchers found one X-linked gene form with strong signs of selection called AMELX, which in other mammals codes for a protein that leads to the mineralization of enamel and regulates other tooth-associated genes. Another gene not on the sex chromosome, MEP1a, also is associated with tusklessness, but not as strongly. This gene, too, is known to be associated with tooth formation in other mammals. Here’s the diagram from the paper of which parts of the tusk are controlled by which gene. You can see that AMELX is expressed only in the “tusky” part of the tusk:

(From paper): Putative functional effects of candidate loci on tusk morphology.A cross section of an African elephant tusk shows the anatomical position of (a) enamel, (b) cementum, (c) dentin (ivory), (d) periodontium, and (e) root of the tusk. Dark blue circles indicate regions known or proposed to be affected by candidate gene AMELX. Light blue circles are proposed to be affected by candidate gene MEP1a. Neither gene is known to affect the formation of the dental pulp (black interior of cross section).

The upshot: Human-imposed (“anthropogenic”) selection that causes evolution in the wild has been demonstrated before, so this phenomenon is not new. What is new is that the genes involved in an anthropogenic evolutionary change—the increase in frequency of the tuskless allele, which is evolution—have been identified for the first time, and we know the kind of selection that’s caused the evolution. What is also unusual (I know of no other case) is that selection for tusklessness is in opposite directions (“antagonistic selection”) in the two sexes so long as tuskless females survive better. As the authors note:

Physical linkage between AMELX and proximate male-lethal loci on the X chromosome, such as HCCS, may underpin the proposed X-linked dominant, male-lethal inheritance of tusklessness in the Gorongosa population. If our interpretation is correct, this study represents a rare example of human-mediated selection favoring a female-specific trait despite its previously unknown deleterious effect in males (sexually antagonistic selection). Given the timeframe of selection, speed of evolutionary response, and known presence of the selected phenotype before the selective event, the selection of standing genetic variation at these loci is the most plausible explanation for the rapid rise of tusklessness during this 15-year period of conflict.

What of the future? Even though the conflict is over, poachers continue to kill tuskers for their ivory in much of Africa. What will happen? We expect the frequency of the dominant tuskless allele to increase. That itself will not lead to extinction of the population because tuskless males are simply not produced: all tuskless females will remain Xx and produce half the normal number of males. Tusked females will still be produced as Xx females crossed to xY males will produce both Xx (tuskless) and xx (tusked) females.  But the reduction in the number of males produced by anthropogenic selection, coupled with continual poaching of both males and females with tusks may drive the population size so low, with an unequal sex ratio, that it could become severely endangered.

Since tusks are good for elephants, the solution is not only to ban the trade in ivory, which has been done in part, but some countries continue to trade in elephant ivory. Further, we must stop the poachers cold, as there’s still a market for both legal and illegal ivory, and prices are high. That’s easier said than done given the area that must be monitored. Note, though, that in 2017, Donald Trump lifted the ban on ivory imports from Zimbabwe, which had been put in place by his predecessor. And the elephant is the Republican symbol!

h/t: Pat, Matt, and several other readers.


S. C. Campbell-Staton et al.. 2021. Ivory poaching and the rapid evolution of tusklessness in elephantsScience 374, 483-487.

Sexual versus natural selection: a case in beetles

October 4, 2021 • 11:15 am

Although Darwin himself drew a bit of a distinction between natural and sexual selection, the latter is really a special case of the former. Sexual selection is simply natural selection among individuals for their ability to acquire a mate: one of many behaviors that determine how many genes you leave behind. And there are cases in which it’s hard to determine which form of selection is going on. If a male’s sperm swim faster than the sperm of other males in a species where females are multiply inseminated (e.g., fruit flies), is that male experiencing positive natural selection or positive sexual selection?

Well, the details don’t matter so long as we keep track of what’s going on. In a new paper in Nature Communications, also summarized in a short News and Views in Current Biology, a group of investigators demonstrate how sexual selection can conflict with other forms of natural selection. The experiment was hard and laborious, but the results can be conveyed simply, and I’ll try.

I’d suggest that if you read one of the two articles, it should be the second, as it’s shorter, written for a less specialized audience, but nevertheless an accurate summary. But if you want the original paper, click on the screenshot below or get the pdf here.

To read the Current Biology precis, click on the screenshot below or get the pdf here. 

We begin with a sexually dimorphic beetle (below), Gnatocerus comutus, the “broad-horned flour beetle” that’s a pest in grain silos.  As you see, it’s sexually dimorphic, with males having bigger heads and, notably, a huge pair of mandibles (arrows). The females lack mandibles. That’s a hint that the mandibles aren’t used for defense against predators or for predation, but are used in male-male competition for females (if they helped procure prey or fight off predators, the females should have them, too). And indeed, that’s exactly what the mandibles are used for.


A prediction from this difference is that there is a metabolic cost to growing those mandibles, and although males with mandibles have higher overall fitness, if you could remove male-male competition, the mandibles wouldn’t give you a selective advantage. In that case they would be selected to evolve a smaller size as the resources used to grow them could be directed at other aspects of fitness. Every time you see a case of sexual dimorphism involving a cumbersome or conspicuous trait, you can predict that that trait has a cost, and is involved in sexual selection (the male peacock’s tail is the classic example).

The authors of the first paper did a clever experiment. Instead of removing male-male competition (you could do this by pairing one male with one female for generations; I predict the mandibles would get smaller), they exposed the males and females (separately) to a vicious predator, the assassin bug Amphibolus venator, which doesn’t regularly prey on G. comutus in nature but will eat anything it encounters.

Here’s the assassin bug confronting its potential prey (from the Current Biology paper):

What happened?

First, over 7 generations, with the males who escaped predation mated to control (unselected) females, the offspring of the escaping males evolved a smaller size. Clearly they weren’t defending themselves against predation from the assassin bugs; rather, the mandibles appear to have been an impediment to survival. The authors suggest that they’re heavy and impede the mobility you need to escape predators.

And, as expected, those small-jawed males whose descendants survived 7 generations of predation lost out when allowed to compete with regular males for females: they won contests only half as often as males from control treatments or female-only predation treatments. Jaws matter at mating time!

What was not expected was that the female descendants of the predated males actually got fitter.  Why? Because their abdomens got larger, possibly enabling them to produce more eggs. (An alternative is that females’ sperm storage organs got larger, enabling them to store more sperm.) But why would this happen? Probably because there is a genetic correlation between male mandible size and, in females, either abdomen or sperm-storage organ size, so if you make the former smaller, the latter get bigger. There’s independent evidence for this. (We don’t know about the developmental pathways that connect male jaws and female abdomens.)

What this shows is not only the cost of sexual selection, but a cost that’s levied in both males and females. If there were no male-male competition, and males had small mandibles, females would leave more offspring.  You might ask, then, given that there are of evolving mandibles paid by both sexes, why do males still evolve large jaws?

The answer must be that the genes that increased male mandible size in the past still had a NET advantage over genes for smaller mandibles. In other words, their cost in reduced ability to escape predators and reduced female offspring number was more than offset by the advantage of winning contests for females. This shows that fitness increases in one sex (the larger mandibles that evolved in males) can be paid for by fitness reductions in the other sex as well (reduced reproductive output of smaller-bellied females).

And so Nature has woven a tangled web here, but one somewhat untangled by the tedious but revealing experiments of the researchers who wrote the first paper.